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Functional alignment of feedback effects from visual cortex to thalamus

Abstract

Following from the classical work of Hubel and Wiesel, it has been recognized that the orientation and the on- and off-zones of receptive fields of layer 4 simple cells in the visual cortex are linked to the spatial alignment and properties of the cells in the visual thalamus that relay the retinal input. Here we present evidence showing that the orientation and the on- and off-zones of receptive fields of layer 6 simple cells in cat visual cortex that provide feedback to the thalamus are similarly linked to the alignment and properties of the receptive fields of the thalamic cells they contact. However, the pattern of influence linked to on- and off-zones is phase-reversed. This has important functional implications.

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Figure 1
Figure 2: Receptive field mapping.
Figure 3: Focal enhancement of cortico-thalamic feedback by iontophoretic application of CGP 55845 (CGP) in layer 6 alters the firing pattern of LGN cells.
Figure 4: Summary of the change in response modes across our LGN sample.
Figure 5: Feedback effects are influenced by the alignment of receptive fields.
Figure 6: Relationship between visual orientation preference and connectivity.

References

  1. Sherman, S.M. Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci. 24, 122–126 (2001).

    Article  CAS  Google Scholar 

  2. Van Horn, S.C., Erisir, A. & Sherman, S.M. Relative distribution of synapses in the A-laminae of the lateral geniculate nucleus of the cat. J. Comp. Neurol. 416, 509–520 (2000).

    Article  CAS  Google Scholar 

  3. Grieve, K.L. & Sillito, A.M. Differential properties of cells in the feline primary visual cortex providing the corticofugal feedback to the lateral geniculate nucleus and visual claustrum. J. Neurosci. 15, 4868–4874 (1995).

    Article  CAS  Google Scholar 

  4. Hubel, D.H. & Wiesel, T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106–154 (1962).

    Article  CAS  Google Scholar 

  5. Reid, R.C. & Alonso, J.M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281–284 (1995).

    Article  CAS  Google Scholar 

  6. Godwin, D.W., Vaughan, J.W. & Sherman, S.M. Metabotropic glutamate receptors switch visual response mode of lateral geniculate nucleus cells from burst to tonic. J. Neurophysiol. 76, 1800–1816 (1996).

    Article  CAS  Google Scholar 

  7. Fanselow, E.E., Sameshima, K., Baccala, L.A. & Nicolelis, M.A. Thalamic bursting in rats during different awake behavioral states. Proc. Natl. Acad. Sci. USA 98, 15330–15335 (2001).

    Article  CAS  Google Scholar 

  8. Ramcharan, E.J., Gnadt, J.W. & Sherman, S.M. Burst and tonic firing in thalamic cells of unanesthetized, behaving monkeys. Vis. Neurosci. 17, 55–62 (2000).

    Article  CAS  Google Scholar 

  9. Rivadulla, C., Martinez, L., Grieve, K.L. & Cudeiro, J. Receptive field structure of burst and tonic firing in feline lateral geniculate nucleus. J. Physiol. (Lond.) 553, 601–610 (2003).

    Article  CAS  Google Scholar 

  10. Sherman, S.M. & Guillery, R.W. Exploring the thalamus (Academic Press, San Diego, 2001).

  11. Brugger, F., Wicki, U., Olpe, H.R., Froestl, W. & Mickel, S. The action of new potent GABAB receptor antagonists in the hemisected spinal cord preparation of the rat. Eur. J. Pharmacol. 235, 153–155 (1993).

    Article  CAS  Google Scholar 

  12. Usrey, W.M., Reppas, J.B. & Reid, R.C. Specificity and strength of retinogeniculate connections. J. Neurophysiol. 82, 3527–3540 (1999).

    Article  CAS  Google Scholar 

  13. Alonso, J.M., Usrey, W.M. & Reid, R.C. Rules of connectivity between geniculate cells and simple cells in cat primary visual cortex. J. Neurosci. 21, 4002–4015 (2001).

    Article  CAS  Google Scholar 

  14. Kara, P. & Reid, R.C. Efficacy of retinal spikes in driving cortical responses. J. Neurosci. 23, 8547–8557 (2003).

    Article  CAS  Google Scholar 

  15. Lu, S.-M., Guido, W. & Sherman, S.M. Effects of membrane voltage on receptive field properties of lateral geniculate neurons in the cat: Contributions of the low-threshold Ca2+ conductance. J. Neurophysiol. 68, 2185–2198 (1992).

    Article  CAS  Google Scholar 

  16. Guido, W. & Weyand, T. Burst responses in thalamic relay cells of the awake behaving cat. J. Neurophysiol. 74, 1782–1786 (1995).

    Article  CAS  Google Scholar 

  17. Ramcharan, E.J., Cox, C.L., Zhan, X.J., Sherman, S.M. & Gnadt, J.W. Cellular mechanisms underlying activity patterns in the monkey thalamus during visual behavior. J. Neurophysiol. 84, 1982–1987 (2000).

    Article  CAS  Google Scholar 

  18. Weyand, T.G., Boudreaux, M. & Guido, W. Burst and tonic response modes in thalamic neurons during sleep and wakefulness. J. Neurophysiol. 85, 1107–1118 (2001).

    Article  CAS  Google Scholar 

  19. Jahnsen, H. & Llinas, R. Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J. Physiol. (Lond.) 349, 205–226 (1984).

    Article  CAS  Google Scholar 

  20. Jahnsen, H. & Llinás, R.R. Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J. Physiol. (Lond.) 349, 227–247 (1984).

    Article  CAS  Google Scholar 

  21. Sherman, S.M. & Guillery, R.W. The role of the thalamus in the flow of information to the cortex. Phil. Trans. R. Soc. Lond. B 357, 1695–1708 (2002).

    Article  Google Scholar 

  22. Murphy, P.C., Duckett, S.G. & Sillito, A.M. Feedback connections to the lateral geniculate nucleus and cortical response properties. Science 286, 1552–1554 (1999).

    Article  CAS  Google Scholar 

  23. Grieve, K.L. & Sillito, A.M. A re-appraisal of the role of layer VI of the visual cortex in the generation of cortical end inhibition. Exp. Brain Res. 87, 521–529 (1991).

    Article  CAS  Google Scholar 

  24. Grieve, K.L. & Sillito, A.M. Non-length-tuned cells in layers II/III and IV of the visual cortex: The effect of blockade of layer VI on responses to stimuli of different lengths. Exp. Brain Res. 104, 12–20 (1995).

    Article  CAS  Google Scholar 

  25. Erwin, E. & Miller, K.D. Correlation-based development of ocularly matched orientation and ocular dominance maps: determination of required input activities. J. Neurosci. 18, 9870–9895 (1998).

    Article  CAS  Google Scholar 

  26. Weliky, M. & Katz, L.C. Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus in vivo. Science 285, 599–604 (1999).

    Article  CAS  Google Scholar 

  27. Cai, D.Q., DeAngelis, G.C. & Freeman, R.D. Spatiotemporal receptive field organization in the lateral geniculate nucleus of cats and kittens. J. Neurophysiol. 78, 1045–1061 (1997).

    Article  CAS  Google Scholar 

  28. Sillito, A.M., Grieve, K.L., Jones, H.E., Cudeiro, J. & Davis, J. Visual cortical mechanisms detecting focal orientation discontinuities. Nature 378, 492–496 (1995).

    Article  CAS  Google Scholar 

  29. Jones, H.E., Wang, W. & Sillito, A.M. Spatial organization and magnitude of orientation contrast interactions in Primate V1. J. Neurophysiol. 88, 2796–2808 (2002).

    Article  CAS  Google Scholar 

  30. Sillito, A.M., Jones, H.E., Gerstein, G.L. & West, D.C. Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex. Nature 369, 479–482 (1994).

    Article  CAS  Google Scholar 

  31. Gerstein, G.L. & Kirkland, K.L. Neural assembles: technical issues, analysis, and modelling. Neural Netw. 14, 589–598 (2001).

    Article  CAS  Google Scholar 

  32. Tsumoto, T., Creutzfeldt, O.D. & Légendy, C.R. Functional organization of the corticofugal system from visual cortex to lateral geniculate nucleus in the cat. Exp. Brain Res. 32, 345–364 (1978).

    Article  CAS  Google Scholar 

  33. Harvey, A.R. A physiological analysis of subcortical and commissural projections of areas 17 and 18 of the cat. J. Physiol. (Lond.) 302, 507–534 (1980).

    Article  CAS  Google Scholar 

  34. Sillito, A.M. & Jones, H.E. Functional organization influencing neurotransmission in the lateral geniculate nucleus in. Thalamus: Volume 2, Experimental and clinical aspects (eds. Steriade, M., Jones, E.G. & McCormick, D.A.) 1–52 (Elsevier, Amsterdam, 1997).

    Google Scholar 

  35. Cudeiro, J. & Sillito, A.M. Spatial frequency tuning of orientation-discontinuity-sensitive corticofugal feedback to the cat lateral geniculate nucleus. J. Physiol. (Lond.) 490, 481–492 (1996).

    Article  CAS  Google Scholar 

  36. Jones, H.E., Grieve, K.L., Wang, W. & Sillito, A.M. Surround suppression in primate V1. J. Neurophysiol. 86, 2011–2028 (2001).

    Article  CAS  Google Scholar 

  37. Enroth-Cugell, C. & Robson, J.G. The contrast sensitivity of retinal ganglion cells of the cat. J. Physiol. (Lond.) 187, 517–552 (1966).

    Article  CAS  Google Scholar 

  38. So, Y.T. & Shapley, R. Spatial tuning of cells in and around lateral geniculate nucleus of the cat: X and Y relay cells and perigeniculate interneurons. J. Neurophysiol. 45, 107–119 (1981).

    Article  CAS  Google Scholar 

  39. Sceniak, M.P., Hawken, M.J. & Shapley, R. Visual spatial characterization of macaque V1 neurons. J. Neurophysiol. 85, 1873–1887 (2001).

    Article  CAS  Google Scholar 

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Acknowledgements

The support of the Medical Research Council is gratefully acknowledged.

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Correspondence to Adam M Sillito.

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Supplementary information

Supplementary Fig. 1

Does the organization of the cortico-thalamic feedback pathway mirror that of the feed-forward geniculo-cortical projection? (PDF 417 kb)

Supplementary Fig. 2

Schematic diagram summarizing the connectivity suggested by the data. (PDF 113 kb)

Supplementary Fig. 3

Reverse Hubel and Wiesel links in feedback from cortex to LGN. (PDF 635 kb)

Supplementary Methods (PDF 136 kb)

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Wang, W., Jones, H., Andolina, I. et al. Functional alignment of feedback effects from visual cortex to thalamus. Nat Neurosci 9, 1330–1336 (2006). https://doi.org/10.1038/nn1768

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